Effects of donepezil on amyloid-β and synapse density in the Tg2576 mouse model of Alzheimer's disease

Brain Research

Volumn 1303, Issue , 2009, Pages 169-178

  Dong, Hongxin ^a   Yuede, Carla M ^a   Coughlan, Carolyn A ^a   Murphy, Keely M ^a   Csernansky, John G ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

Author keywords

Alzheimer's disease; Amyloid; Donepezil; Synapse density; Synaptophysin; Tg2576 mice

Indexed keywords

AMYLOID BETA PROTEIN; AMYLOID BETA PROTEIN[1-40]; AMYLOID BETA PROTEIN[1-42]; DONEPEZIL; SYNAPTOPHYSIN;

ALZHEIMER DISEASE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN TISSUE; CONTROLLED STUDY; DENTATE GYRUS; ELECTRON MICROSCOPY; FEMALE; HIPPOCAMPUS; MALE; MOUSE; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; SYNAPSE;

ALZHEIMER DISEASE; AMYLOID BETA-PROTEIN; AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; BIOLOGICAL MARKERS; CHOLINESTERASE INHIBITORS; DENTATE GYRUS; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG ADMINISTRATION SCHEDULE; HIPPOCAMPUS; HUMANS; INDANS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MICROSCOPY, ELECTRON, TRANSMISSION; NEUROPROTECTIVE AGENTS; PIPERIDINES; SENILE PLAQUES; SYNAPSES; SYNAPTOPHYSIN; TIME; TREATMENT OUTCOME;

MUS;

EID: 71849085520     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2009.09.097     Document Type: Article

References (64)

1. Akaike A. Preclinical evidence of neuroprotection by cholinesterase inhibitors. Alzheimer Dis. Assoc. Disord. 20 (2006) S8-11
2. Akasofu S., Kosasa T., Kimura M., and Kubota A. Protective effect of donepezil in a primary culture of rat cortical neurons exposed to oxygen-glucose deprivation. Eur. J. Pharmacol. 472 (2003) 57-63
3. Akasofu S., Kimura M., Kosasa T., Sawada K., and Ogura H. Study of neuroprotection of donepezil, a therapy for Alzheimer's disease. Chem. Biol. Interact. 175 (2008) 222-226
4. Apelt J., Kumar A., and Schliebs R. Impairment of cholinergic neurotransmission in adult and aged transgenic Tg2576 mouse brain expressing the Swedish mutation of human beta-amyloid precursor protein. Brain Res. 953 (2002) 17-30
5. Birks J., and Harvey R.J. Donepezil for dementia due to Alzheimer's disease. Cochrane Database Syst. Rev. 25 (2006) 1-284
6. Bannerman D.M., Yee B.K., Lemaire M., Wilbrecht L., Jarrard L., Iversen S.D., Rawlins J.N., and Good M.A. The role of the entorhinal cortex in two forms of spatial learning and memory. Exp. Brain Res. 141 (2001) 281-303
7. Barnes P., and Good M. Impaired Pavlovian cued fear conditioning in Tg2576 mice expressing a human mutant amyloid precursor protein gene. Behav. Brain Res. 157 (2005) 107-117
8. Bartolini M., Bertucci C., Vavrini V., and Andrisano V. beta-Amyloid aggregation induced by human acetylcholinesterase: Inhibition studies. Biochem. Pharmacol. 65 (2003) 407-416
9. Bonthius D.J., Bonthius N.E., Napper R.M., and West J.R. Early postnatal alcohol exposure acutely and permanently reduces the number of granule cells and mitral cells in the rat olfactory bulb: a stereological study. J. Comp. Neurol. 324 (1992) 557-566
10. Bonthius D.J., McKim R., Koele L., Harb H., Karacay B., Mahoney J., and Pantazis N.J. Use of frozen sections to determine neuronal number in the murine hippocampus and neocortex using the optical dissector and optical fractionator. Brain Res. Protoc. 14 (2004) 45-57
11. Capsoni S., Giannotta S., Stebel M., Garcia A.A., De Rosa R., Villetti G., Imbimbo B.P., Pietra C., and Cattaneo A. Ganstigmine and donepezil improve neurodegeneration in AD11 antinerve growth factor transgenic mice. Am. J. Alzheimers Dis. Other Demen. 19 (2004) 153-160
12. Chapman P.F., White G.L., Jones M.W., Cooper-Blacketer D., Marshall V.J., Irizarry M., Younkin L., Good M.A., Bliss T.V., Hyman B.T., Younkin S.G., and Hsiao K.K. Impaired synaptic plasticity and learning in aged amyloid precursor protein transgenic mice. Nature Neurosci. 2 (1999) 271-276
13. Creeley C.E., Wozniak D.F., Nardi A., Farber N.B., and Olney J.W. Donepezil markedly potentiates memantine neurotoxicity in the adult rat brain. Neurobiol. Aging 29 (2008) 153-167
14. Csernansky J., Bargett M., Dong H., Humphrey W., and Wang L. Hippocampal structure and the action of cholinomimetic drugs. Drug Dev. Res. 51 (2002) 1-10
15. Davis K.L., Thal L.J., Gamzu E.R., Davis C.S., Woolson R.F., Gracon S.I., Drachman D.A., Schneider L.S., Whitehouse P.J., and Hoover T.M. The Tacrine Collaborative Study Group. A double-blind placebo controlled multicenter study of tacrine for Alzheimer's disease. N. Engl. J. Med. 327 (1992) 1253-1259
16. Dong H., Csernansky C.A., Martin M.V., Bertchume A., Vallera D., and Csernansky J.G. Acetylcholinesterase inhibitors ameliorate behavioral deficits in the Tg2576 mouse model of Alzheimer's disease. Psychopharmacology (Berl) 181 (2005) 145-152
17. Dong H., Martin M.V., Chambers S., and Csernansky J.G. Spatial relationship between synapse loss and beta-amyloid deposition in Tg2576 mice. J. Comp. Neurol. 500 (2007) 11-321
18. Dong H., Yuede C.M., Coughlan C., Lewis B., and Csernansky J.G. Effects of memantine on neuronal structure and conditioned fear in the Tg2576 mouse model of Alzheimer's disease. Neuropsychopharmacology 33 (2008) 3226-3236
19. Floden A.M., Li S., and Combs C.K. beta-Amyloid-stimulated microglia induce neuron death via synergistic stimulation of tumor necrosis factor alpha and NMDA receptors. J. Neurosci. 25 (2005) 2566-2575
20. Francis P.T., Palmer A.M., Snape M., and Wilcock G.K. The cholinergic hypothesis of Alzheimer's disease: a review of progress. J. Neurol. Neurosurg. Psychiatry 66 (1999) 137-147
21. Frisch C., Hüsch K., Angenstein F., Kudin A., Kunz W., Elger C.E., and Helmstaedter C. Dose-dependent memory effects and cerebral volume changes after in utero exposure to valproate in the rat. Epilepsia 50 (2009) 1432-1441
22. Fujiki M., Kubo T., Kamida T., Sugita K., Hikawa T., Abe T., Ishii K., and Kobayashi H. Neuroprotective and antiamnesic effect of donepezil, a nicotinic acetylcholine-receptor activator, on rats with concussive mild traumatic brain injury. J. Clin. Neurosci. 15 (2008) 791-796
23. Geinisman Y., Disterhoft J.F., Gundersen H.J., McEchron M.D., Persina I.S., Power J.M., van der Zee E.A., and West M.J. Remodeling of hippocampal synapses after hippocampus-dependent associative learning. J. Comp. Neurol. 417 (2000) 49-59
24. Giacobini E. Do cholinesterase inhibitors have disease-modifying effects in Alzheimer's disease?. CNS Drugs 15 (2001) 85-91
25. Greig N.H., Utsuki T., Ingram D.K., Wang Y., Pepeu G., Scali C., Yu Q.S., Mamczarz J., Holloway H.W., Giordano T., Chen D., Furukawa K., Sambamurti K., Brossi A., and Lahiri D.K. Selective butyrylcholinesterase inhibition elevates brain acetylcholine, augments learning and lowers Alzheimer beta-amyloid peptide in rodent. Proc. Natl. Acad. Sci. U.S.A. 102 (2005) 17213-17218
26. Guntern E., Bouras C., Hoff P.R., and Vallet P.G. An improved thioflavine S method for staining neurofibrillary tangles ad senile plaques in Alzheimer's disease. Experientia 48 (1992) 8-10
27. Handattu S.P., Garber D.W., Monroe C.E., van Groen T., Kadish I., Nayyar G., Cao D., Palgunachari M.N., Li L., and Anantharamaiah G.M. Oral apolipoprotein A-I mimetic peptide improves cognitive function and reduces amyloid burden in a mouse model of Alzheimer's disease. Neurobiol. Dis. 34 (2009) 525-534
28. Hansen R.A., Gartlehner G., Webb A.P., Morgan L.C., Moore C.G., and Jonas D.E. Efficacy and safety of donepezil, galantamine, and rivastigmine for the treatment of Alzheimer's disease: a systematic review and meta-analysis. Clin. Interv. Aging 3 (2008) 211-225
29. Hsiao K. Learning and memory in transgenic mice modeling Alzheimer's disease. Learn. Mem. 8 (2001) 301-308
30. Hsiao K., Chapman P., Nilsen S., Eckman C., Harigaya Y., Younkin S., Yang F., and Cole G. Correlative memory deficits, Aβ elevation and amyloid plaques in transgenic mice. Science 274 (1996) 99-102
31. Inestrosa N.C., Alvarez A., Perez C.A., Moreno R.D., Vicente M., Linker C., Casanueva O.I., Soto C., and Garrido J. Acetylcholinesterase accelerates assembly of amyloid-β-peptides into Alzheimer's fibrils: possible role of the peripheral site of the enzyme. Neuron 16 (1996) 881-891
32. Irizarry M., McNamara M., Fedorchak K., Hsiao K., and Hyman B. APPsw transgenic mice develop age-related Ab deposits and neuropil abnormalities, but no neuronal loss in CA1. J. Neuropath. Exper. Neurol. 56 (1997) 965-973
33. Knowles W.D. Normal anatomy and neurophysiology of the hippocampal formation. J. Clin. Neurophysicol. 9 (1992) 252-263
34. Kimura M., Akasofu S., Ogura H., and Sawada K. Comparison of donepezil and memantine for protective effect against amyloid-beta(1-42) toxicity in rat septal neurons. Brain Res. 1047 (2005) 72-84
35. Kimura M., Komatsu H., Ogura H., and Sawada K. Protective effect of donepezil against Abeta(1-40) neurotoxicity in rat septal neurons. Neurosci. Lett. 391 (2005) 17-21
36. King D.L., and Arendash G.W. Maintained synaptophysin immunoreactivity in Tg2576 transgenic mice during aging: correlations with cognitive impairment. Brain Res. 926 (2002) 58-68
37. Mori E., Hashimoto M., Krishnan K.R., and Doraiswamy P.M. What constitutes clinical evidence for neuroprotection in Alzheimer disease: support for the cholinesterase inhibitors?. Alzheimer Dis. Assoc. Disord. Suppl. 1 (2006) S19-26
38. Nilsberth C., Basun H., Eckman C., Lannfelt L., and Younkin S. Plasma levels of Ab42 and Ab40 in Alzheimer patients during treatment with the acetylcholinesterase inhibitor tacrine. Dement. Geriatr. Cogn. Disord. 14 (2002) 156-160
39. Nitsch R.M., Slack B.E., Wurtman R.J., and Growdon J.H. Release of Alzheimer amyloid precursor derivatives stimulated by activation of muscarinic acetylcholine receptors. Science 258 (1992) 304-307
40. Phinney A.L., Calhoun M.E., Wolfer D.P., Lipp H.P., Zheng H., and Jucker M. No hippocampal neuron or synaptic bouton loss in learning-impaired aged beta-amyloid precursor protein-null mice. Neuroscience 90 (1999) 1207-1216
41. Probst A., Basler V., Bron B., and Ulrich J. Neuritic plaques in senile dementia of Alzheimer type: a Golgi analysis in the hippocampal region. Brain Res. 268 (1983) 249-254
42. Reilly J.F., Games D., Rydel R.E., Freedman S., Schenk D., Young W.G., Morrison J.H., and Bloom F.E. Amyloid deposition in the hippocampus and entorhinal cortex: quantitative analysis of a transgenic mouse model. Proc. Natl. Acad. Sci. U. S. A. 100 (2003) 4837-4842
43. Rogers S.L., Farlow M.R., Doody R.S., Mohs R., and Friedhoff L.T. A 24-week, double-blind, placebo-controlled trial of donepezil in patients with Alzheimer's disease. Neurology 50 (1998) 136-145
44. Rogers S.L., Doody R.S., Mohs R.C., and Friedhoff L.T. Donepezil improves cognition and global function in Alzheimer disease: a 15-week, double-blind, placebo-controlled study. Donepezil Study Group. Arch Intern Med. 158 (1998) 1021-1031
45. Roselli F., Tirard M., Lu J., Hutzler P., Lamberti P., Livrea P., Morabito M., and Almeida O.F. Soluble beta-amyloid1-40 induces NMDA-dependent degradation of postsynaptic density-95 at glutamatergic synapses. J. Neurosci. 30 (2005) 11061-11070
46. Rutten B.P., Van der Kolk N.M., Schafer S., van Zandvoort M.A., Bayer T.A., Steinbusch H.W., and Schmitz C. Age-related loss of synaptophysin immunoreactive presynaptic boutons within the hippocampus of APP751SL, PS1M146L, and APP751SL/PS1M146L transgenic mice. Am. J. Pathol. 167 (2005) 161-173
47. Saxena G., Singh S.P., Agrawal R., and Nath C. Effect of donepezil and tacrine on oxidative stress in intracerebral streptozotocin-induced model of dementia in mice. Eur. J. Pharmacol. 10 581 (2008) 283-289
48. Snyder E.M., Colledge M., Crozier R.A., Chen W.S., Scott J.D., and Bear M.F. J. Biol. Chem. 280 (2005) 16962-16968
49. Spires T.L., Meyer-Luehmann M., Stern E.A., McLean P.J., Skoch J., Nguyen P.T., Bacskai B.J., and Hyman B.T. Dendritic spine abnormalities in amyloid precursor protein transgenic mice demonstrated by gene transfer and intravital multiphoton microscopy. J. Neurosci. 25 (2005) 7278-7287
50. Spowart-Manning L., and van der Staay F.J. The T-maze continuous alternation task for assessing the effects of putative cognition enhancers in the mouse. Behav. Brain Res. 151 (2004) 37-46
51. Stern E.A., Bacskai B.J., Hickey G.A., Attenello F.J., Lombardo J.A., and Hyman B.T. Cortical synaptic integration in vivo is disrupted by amyloid-beta plaques. J. Neurosci. 24 (2004) 4535-4540
52. Sturchler-Pierrat C., Abramowski D., Duke M., Wiederhold K.H., Mistl C., Rothacher S., Ledermann B., Burki K., Frey P., Paganetti P.A., Waridel C., Calhoun M.E., Jucker M., Probst A., Staufenbiel M., and Sommer B. Two amyloid precursor protein transgenic mouse models with Alzheimer disease-like pathology. Proc. Natl. Acad. Sci. U.S.A. 94 (1997) 13287-13292
53. Su Y., and Ni B. Selective deposition of amyloid-protein in the entorhinal-dentate projection of a transgenic mouse model of Alzheimer's disease. J. Neurosci. Res. 53 (1998) 177-186
54. Takada Y., Yonezawa A., Kume T., Katsuki H., Kaneko S., Sugimoto H., and Akaike A. Nicotinic acetylcholine receptor-mediated neuroprotection by donepezil against glutamate neurotoxicity in rat cortical neurons. J. Pharmacol. Exp. Ther. 306 (2003) 772-777
55. Takada-Takatori Y., Kume T., Izumi Y., Ohgi Y., Niidome T., Fujii T., Sugimoto H., and Akaike A. Roles of nicotinic receptors in acetylcholinesterase inhibitor-induced neuroprotection and nicotinic receptor up-regulation. Biol. Pharm. Bull. 32 (2009) 318-324
56. Tariot P.N., Solomon P.R., Morris J.C., Kershaw P., Lilienfeld S., and Ding C. Galantamine USA-10 Study Group. A 5-month randomized placebo-controlled trial of galantamine in AD. Neurology 54 (2000) 2269-2276
57. Tyszkiewicz J.P., and Yan Z. beta-Amyloid peptides impair PKC-dependent functions of metabotropic glutamate receptors in prefrontal cortical neurons. J. Neurophysiol. 93 (2005) 3102-3111
58. West M., and Gundersen H. Unbiased stereological estimation of the number of neurons in the human hippocampus. J. Comp. Neurol. 296 (1990) 1-22
59. West M.J., Slomianka L., and Gundersen H.J. Unbiased stereological estimation of the total number of neurons in the subdivisions of the rat hippocampus using the optical fractionator. Anat. Rec. 231 (1991) 482-497
60. West M.J., Kawas C.H., Stewart W.F., Rudow G.L., and Troncoso J.C. Hippocampal neurons in pre-clinical Alzheimer's disease. Neurobiol. Aging 25 (2004) 1205-1212
61. Wiedenmann B., and Franke W.W. Identification and localization of synaptophysin, an integral membrane glycoprotein of Mr 38,000 characteristic of presynaptic vesicles. Cell 41 (1985) 1017-1028
62. Yuede C.M., Dong H., and Csernansky J.G. Anti-dementia drugs and hippocampal-dependent memory in rodents. Behav. Pharmacol. 18 (2007) 347-363
63. Zimmermann M., Gardoni F., Marcello E., Colciaghi F., Borroni B., Padovani A., Cattabeni F., and Di Luca M. Acetylcholinesterase inhibitors increase ADAM10 activity by promoting its trafficking in neuroblastoma cell lines. J. Neurochem. 90 (2004) 1489-1499
64. Zhou J., Fu Y., and Tang X.C. Huperzine A and donepezil protect rat pheochromocytoma cells against oxygen-glucose deprivation. Neurosci. Lett. 306 (2001) 53-56